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Tick-Borne Pathogens and Spread of Ixodes ricinus in Lithuania

 Rediger
  Published: 20.07.09 Updated: 20.07.2009 10:48:19

M. Žygutienė
Centre for Communicable Diseases Prevention and Control, Vilnius, Lithuania

Citation: Žygutienė M. Tick-Borne Pathogens and Spread of Ixodes ricinus in Lithuania.  EpiNorth.2009;10(2):63-71.

Abstract
Ticks are among the most widely distributed blood-sucking arthropods in nature. The main threat ticks pose to humans is their role as vectors of various pathogens that may cause disease, the most important in the European region being tick-borne encephalitis (TBE) and Lyme disease. Both diseases are transmitted by hard ticks of the Ixodes species, and Ixodes ricinus predominates in Europe. The main vector of tick-borne diseases in Lithuania is Ixodes ricinus, a tick that is found in temperate regions in Europe. In Lithuania 3,232 cases of TBE and 14,926 cases of Lyme disease were reported during 2000 – 2008. A significant rise of morbidity has been seen in the last 12 years (1997-2008). The highest incidence of tick-borne diseases was registered in 2003 with 763 TBE (22 per 100,000 population) and 3,688 Lyme disease cases (106 per 100,000 population). TBE virus has been found in ticks from 221 localities and B. burgdorferi sensu lato from 150 localities of Lithuania. In addition to TBE virus and B. burgdorferi sensu lato, bacteria Anaplasma, two species of protozoa (Babesia, Trypanosoma) and relapsing fever group spirochete B. miyamotoi were detected in I. ricinus ticks in Lithuania.

Introduction
Tick-borne diseases are present within Europe and are widespread such as Lyme disease or focal such as tick-borne encephalitis (TBE) depending on interactions between the environment, parasites, ticks, and vertebrate hosts. Environmental factors, public health activities and recent changes in the economic, social and political environments of Europe have resulted in tick-borne diseases across the continent (1, 2, 4).

TBE is the most important and widespread of the arboviruses transmitted by ticks in Europe (4). TBE is caused by a single-stranded RNA flavivirus related to the yellow fever, dengue, Japanese encephalitis, and West Nile viruses. According to the International Committee for Taxonomy of Viruses, TBE virus is classified as one species with three subtypes, namely the European subtype (that comprises almost all known isolates from Europe), the Siberian subtype (mainly isolates from the Urals, Siberia and far-eastern Russia) and the Far Eastern subtype (mainly isolates from far-eastern Russia, China and Japan) (5).

Lyme disease is the most commonly reported tick-borne infection in Europe and North America. The disease is a multi-system disorder that can affect a complex range of tissues including the skin, heart, nervous system, eyes, kidneys, and liver. The causative agent Borrelia burgdorferi can be divided into at least ten species: B. burgdorferi sensu stricto (present in Europe and in the USA), B. garinii, B. afzelii, B. valaisiana and B. lusitaniae (Eurasia), B. japonica, B. tanukii and B. turdae (Japan) and B. andersonii and B. bissettii (USA). Other borrelias transmitted by hard ticks have been identified in the USA (B. lonestari) and Japan (B. miyamotoi). Furthermore, the causative agent of Crimean Congo haemorrhagic fever and other tick-borne viruses like Thogoto, Dhori, Tribec, Tettnang, Eyach have been reported in Europe (4).

The tick-borne rickettsial diseases reported in Europe include the spotted fevers, ehrlichiosis, rickettsial pox and Q fever (4). I. ricinus is a vector of emerging zoonotic pathogens including Babesia spp. and Bartonella spp. Co-infection of Bartonella spp. with known tick-borne pathogens such as B. burgdorferi sensu lato, A. phagocytophilum, or Babesia spp. is not a rare event in ticks and hosts (6).

This article summarises epidemiological data, data on tick distribution and the prevalence of pathogens in ticks during 1991-2008 in Lithuania.

Materials and methods
Ixodes ricinus ticks were sampled from woodlands by the flagging method, dragging flannel flags over the vegetation from different locations of Lithuania. All collected ticks were placed into tubes and stored alive at 5º C until they were examined for the presence of B. burgdorferi and Trypanosoma in bowel smears.

From 1970 till 1989 TBE virus isolation was performed in suckling mice, later in cell culture (SPEV pig embryo kidney) and then identified by an indirect immunofluoresence method. Since 2001, ticks have been tested by polymerase chain reaction (PCR). PCR has also been used for the identification of Borrelia parasites and genospecies of Anaplasma and Babesia.

Data including morbidity, localities where people acquired infection and incidence of tick density was obtained from official reports at the Centre for Communicable Diseases Prevention and Control, Lithuania.

Results and discussion
I.ricinus is spread throughout Lithuania and it is the main vector of TBE and Lyme disease. The largest abundance of ticks (52-129 ticks per 1 km of  road) was observed in the central part of Lithuania, where the highest incidence of TBE is reported (Figure 1).

Fig. 1. I. ricinus density (number per 1 km of road) during spring activity, Lithuania 2005

Fig. 1. I. ricinus density (number per 1 km of road) during spring activity, Lithuania 2005

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The observation point for tick counting in Klaipeda was established in 1987 and is still functioning. Seasonal changes in tick abundance were observed there (Figure 2).

Fig. 2. Ixodes ricinus (adults+nymphs) abundance in Klaipeda (observation site: Giruliu forest) in 1995, 2007 and 2008

Fig. 2. Ixodes ricinus (adults+nymphs) abundance in Klaipeda (observation site: Giruliu forest) in 1995, 2007 and 2008

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The tick density during spring peak of activity increased three times from 1995 (19 ticks/1 km) until 2008 (57 ticks/1 km). There was an unusual autumn peak of activity for I.ricinus in 2008. This was the highest reported tick density for September, and was probably a result of favourable weather conditions. Seasonal precipitation during summer and autumn was 209 mm and 174 mm, respectively (close to the norm). Average air temperature in September varied from 7.1 to 23.1 ºC (Lithuanian Hydrometeorological Service). The survival and development of ticks under such conditions was favorable.

Another evident change is an increased period of the time of tick activity. The last ticks in 2007 were gathered in the middle of December and the first in 2008 in the middle of March. No ticks were found during the three winter months. Unusual tick activity increases the risk of infectious tick bites, especially if visitors to forests do not expect ticks to be active at a particular time of the year (1).

Russia, Latvia, Estonia, and Lithuania are considered endemic countries for tick-borne zoonoses (2, 5). TBE and Lyme disease are present in all districts of Lithuania. From 2000 until 2008 a total of 3,232 cases of tick-borne encephalitis (TBE) were reported in Lithuania and a significant rise in morbidity has been reported during the last 12 years (1997-2008). In 2003, the epidemiology of tick-borne diseases in Lithuania was very unusual. The incidence rate of TBE (763 cases, 22 per 100,000 inhabitants) was twice the average incidence over the last ten years, and the highest annual rate recorded since notification was introduced at the end of the 1960s. The 2003 rate for TBE and Lyme disease (3,688 cases, 106 per 100,000 inhabitants) in Lithuania was the highest of all Baltic countries. The TBE incidence was 6.9 in 2007 as compared to 13.5 in 2006; Lyme disease was 41.0 and 59.4, respectively (Figure 3).

Fig. 3. Incidence of Lyme disease and TBE and average annual density index of Ixodes ricinus at observation points, Lithuania, 1991 – 2008

Fig. 3. Incidence of Lyme disease and TBE and average annual density index of Ixodes ricinus at observation points, Lithuania, 1991 – 2008

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The spring and summer in Lithuania was very hot and dry in 2002. The mean spring temperature was 7.9 - 9.2°C. Such a high temperature has not observed during the last 100 years. The mean summer temperature reached 18.2 – 19.5°C and may have curbed tick activity. The lowest average annual incidence was observed, 11 ticks per 1 km of road during this season.

From 17.2 to 32.2% of all TBE cases were infected in the northern and central parts of the country, mainly in the Kaunas, Panevezys and Siauliai regions (Figure 4). From 1.7 to 6.6% of the cases were caught in other regions of Lithuania, 0.7% contracted the infection abroad and the origin of 8.5% of the cases was unknown.

Fig. 4. Geographical distribution of territories where people were infected with TBE in Lithuania during  2000-2008 (n=3,232 cases)

Fig. 3. Incidence of Lyme disease and TBE and average annual density index of Ixodes ricinus at observation points, Lithuania, 1991 – 2008

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Fig. 5. Geographical distribution of territories where people were infected with Lyme disease in Lithuania during 2000-2008 (n=14,926 cases)

Fig. 5. Geographical distribution of territories where people were infected with Lyme disease in Lithuania during 2000-2008 (n=14,926 cases

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

In most cases people caught Lyme disease in the regions around the towns Vilnius, Kaunas, and Panevezys. People usually became infected while visiting tick-infected habitats for work, picking of berries, mushrooms and herbs or leisure.

According to several published studies, TBE virus has been found in ticks collected from 221 localities and B. burgdorferi sensu lato from 150 localities of Lithuania. TBE virus was isolated from ticks collected in all administrative regions and in three urban parks in Lithuania. In addition to TBE virus and Borrelia burgdorferi sensu lato, Anaplasma bacteria and two species of protozoa belonging Babesia and Trypanosoma were detected in I. ricinus ticks.

During 2001 the prevalence of the TBE virus in tick pools was 1.4%, ranging from 1.0 % in Panavežys, 0.4% in Šiauliai and 1.7% in Radviliškis. Sequence analysis showed that the virus belonged to the Western TBE lineage (8).

The mean B.burgdorferi sensu lato infection prevalence of I. ricinus ticks in Lithuania was 13.4%, ranging from 1 % to 35% in different locations. All three Borrelia genospecies were detected in ticks: B. afzelii (9-10%), B. garinii (2.5-5.0%) and B.burgdorferi sensu stricto (0.4%). In contrast, all four pathogenic genospecies of B. burgdorferi sensu lato are present in Europe, although most of the Lyme disease cases are caused by B. afzelii and B. garinii. B. afzelii predominates in the northern, central and eastern parts of Europe, and B. garinii in the western parts (7).

The ticks were positive for Ehrlichia/Anaplasma (5%), B.burgdorferi sensu lato (0.4%) and Babesia divergens (2%) (9-13). Trypanasome (amastigotae, promastigote and epimastigote) were identified among 0.1% of the I. ricinus examined (14).

In 2005, B. miyamotoi had an infection rate of 1.5% (13). Rickettsia slovaca, Coxiella burnetii and Uukuniemi virus were detected in ticks in the end of 1970. (15,16). In addition to I.ricinus, Dermacentor reticulatus has been observed in Lithuania. The population distribution of this species has expanded during recent years. D.reticulatus is a competent vector for pathogens including Francisella tularensis, Coxiella burnetti, Babesia, Bartonella and Anaplasma marginale (1).

Zoonotic tick-borne diseases in Europe have increased dramatically since early 1980s, and the incidence of TBE and Lyme disease has risen over the last two decades (1). Both diseases are transmitted by Ixodes spp., a vector of medical importance, great abundance and wide distribution.

I .ricinus is exophilic, passively questing from vegetation for its hosts, which include a wide range of reptiles, birds and mammals (3). The geographical distribution of Lyme disease worldwide correlates with the known distribution of the ixodid vectors. Climate determines the latitudinal and altitudinal distribution of ticks. During the last decades ticks have spread into higher latitudes (observed in Sweden) and altitudes (observed in the Czech Republic) in Europe and have become more abundant in many places. These tick distribution and density changes have been shown to be related to changes in climate. The incidences of Lyme disease and other tick-borne diseases have also increased in Europe during the same time period. (7)

Gray et al. (1) maintain that climate change may also be partly responsible for the change in distribution of D. reticulatus. The life cycle of this species of tick is much shorter than that of the I. ricinus, with eggs deposited in the spring and developing to adults within the same year. The geographic range of D. reticulatus extends from France and southwest England in the west to central Asia in the east. The northern limit is northern Germany, northern Poland and Lithuania in western and central Europe (1).

Several factors could be responsible for the recent spread of D. reticulatus including increased deer abundance and the availability of more neglected land as a result of EU agricultural policies (1). Even though ticks feed on a large range of species including mammals, birds and reptiles, only a few may act as reservoirs for the pathogen. The abundance of reservoir hosts in a particular habitat is the most important factor in the establishment of infected tick populations (7).

The leafy forest is dominant in central and northern Lithuania where the largest abundance of tick is observed and high incidence of TBE is reported. There has been an increase in the number of wild animals, for instance elk with the numbers of animals increasing from 1,100 in 1960 to 4,092 in 2003 and almost a threefold increase the roe deer population to 72,945 animals during the same period (Ministry of Environment of Lithuania).

Lyme disease is the most common vector-borne disease in temperate zones of the northern hemisphere. Approximately 85,000 cases are reported annually in Europe. Climatic conditions, except for unusually high temperatures, have little influence. However, human exposure to the pathogen through tick bites may be influenced by weather conditions (7).

The economic crisis in the 1990s, changes in the agricultural and industrial sectors had consequences for environmental and socio-economic conditions, many of which could have affected both the abundance of infected ticks and contact of humans with those ticks. These changes acted with climate factors to increase TBE incidence (17).

Conclusion
The epidemiological importance of tick-borne diseases in Lithuania is similar to that in other countries of Central Europe. Agents of infectious diseases transmitted by ticks, such as TBE virus and B. burgdorferi sensu lato are serious hazard to human health. Ongoing research in tick-borne diseases will help to assess reasons of the distribution of these zoonoses. Occurrence of new pathogen in ticks has to be taken into account in future surveys. The differences in the timing of ticks activity and abundance sustain opinion that understanding of nature’s process requires long-term investigations.

References

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